Alternative cell death mechanisms determine epidermal resistance in incompatible barley-Ustilago interactions

Programmed cell death is a key feature of epidermal plant immunity, which is particularly effective against biotrophic microbes that depend on living host tissue. The covered smut fungus Ustilago hordei establishes a compatible biotrophic interaction with its host plant barley. The maize smut U. maydis triggers a nonhost response in barley, which results in epidermal cell death. Similarly, Ustilago mutants being deleted for pep1, a gene encoding a secreted effector, are blocked upon host penetration. We studied the epidermal responses of barley to incompatible Ustilago strains. Molecular and cellular analyses were used to test the impact of Bax inhibitor-1 (BI-1), a suppressor of programmed cell death, on the barley nonhost resistance to U. maydis as well as Ustilago Δpep1 mutants. Overexpression of BI-1 resulted in partial break of barley nonhost resistance to U. maydis. By contrast, the epidermal cell death response triggered by pep1 deletion mutants was not impaired by BI-1. Hypersensitive-response-like cell death caused by U. maydis wild-type infection showed features of necrotic cell death, while Δpep1 mutant-induced host responses involved hallmarks of autophagy. Therefore, we propose that the mechanisms of epidermal cell death in response to different types of incompatible pathogens depend on spatial and temporal appearance of cell-death-triggering stimuli.